Skip to main content
SpringerLink
Log in

Phase shifting a circadian rhythm in the eye ofAplysia by high potassium pulses

  • Published:
Journal of comparative physiology Aims and scope Submit manuscript

Summary

  1. 1.

    The circadian rhythm of spontaneous optic nerve impulses from the isolated eye ofAplysia californcía was studied. A general hypothesis was investigated: light-dark cycles, which can entrainin vitro the rhythm from the eye, couple to the intracellular clock mechanism through membrane depolarization. This hypothesis was tested by exposing isolated eyes for fixed durations of time to a depolarizing stimulus, namely, elevation of K +0 (hi-K pulses).

  2. 2.

    Depending on the phase of the rhythm in at which the eyes were treated, hi-K pulses produced either advance or delay phase shifts in the rhythm. A phase response curve was thus generated for 107 mM k +0 pulses of 4 hr duration.

  3. 3.

    If the duration of the hi-K pulse was varied, keeping the phase at which the pulse started constant, the magnitude of the phase shift varied in a linear manner with the duration of the pulse.

  4. 4.

    To examine the involvement of transmitter and neurohormone release in the production of the phase shifts, eyes were exposed to hi-K pulses in the presence of a medium (high Mg++, low Ca++) which should inhibit such release. Since only slight differences were observed in the phase shifts produced by hi-K and by hi-K in the presence of high Mg++, low Ca++, transmitter and neurohormone release do not appear to be involved in phase shift production by hi-K. It is likely that membrane depolarization alone is responsible for the phase shifts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abood, L. G.: Interrelationships between phosphates and calcium in bioelectric phenomena. Internat. Rev. Neurobiol.9, 223–261 (1966).

    Google Scholar 

  • Arch, S.: Polypeptide secretion from the isolated parieto-visceral ganglion ofAplysia Californica. J. gen. Physiol.59, 47–59 (1972).

    Google Scholar 

  • Audesirk, G.: Neuronal interactions in optic nerve impulse production inAplysia. Physiologist14, 105 (1971).

    Google Scholar 

  • Austin, G., Yai, H., Sato, M.: Calcium ion effects onAplysia membrane potentials. In: Invertebrate nervous systems (C. A. G. Wiersma, ed.), p. 39–53. Chicago: Univ. of Chicago Press 1967.

    Google Scholar 

  • Baker, P. F.: Recent experiments on the properties of the Na efflux from squid axons. J. gen. Physiol.51 (part 2), p. 172–179 (1968).

    Google Scholar 

  • Baker, P. F., Connelly, C. M.: Some properties of the external activation site of the Na pump in crab nerve. J. Physiol. (Lond.)185, 270–297 (1966).

    Google Scholar 

  • Berlind, A., Cooke, I. M.: The role of divalent cations in electrically excited release of a neurohormone from crab pericardial organs. Gen. comp. Endocrinol.17, 60–72 (1971).

    Google Scholar 

  • Brink, F. Jr., Bronk, D. W., Larrabee, M. G.: Chemical excitation of nerve. Ann. N.Y. Acad. Sci.47, 457–485 (1946).

    Google Scholar 

  • Carpenter, D. O., Alving, B. O.: A contribution of an electrogenic Na+ pump to membrane potential inAplysia neurons. J. gen. Physiol.52, 1–21 (1968).

    Google Scholar 

  • Carpenter, D. O., Gunn, R.: The dependence of pacemaker discharge ofAplysia neurons upon Na+ and Ca++. J. cell. Physiol.75, 121–127 (1970).

    Google Scholar 

  • Curtis, H. J., Cole, K. S.: Membrane resting and action potentials from the squid giant axon. J. cell. comp. Physiol.19, 135–144 (1942).

    Google Scholar 

  • Engbaek, L.: The pharmacological actions of magnesium ions with particular reference to the neuromuscular and cardiovascular system. Pharmacol. Rev.4, 396–414 (1952).

    Google Scholar 

  • Eskin, A.: Properties of theAplysia visual system:in vitro entrainment of the circadian rhythm and centrifugal regulation of the eye. Z. vergl. Physiol.74, 353–371 (1971).

    Google Scholar 

  • Frankenhaeuser, B., Vallbo, A. B.: Accommodation in myelinated nerve fibers ofXenopus laevis as computed on the basis of valtage clamp data. Acta physiol. scand.63, 1–20 (1965).

    Google Scholar 

  • Gorman, A. L. F., Marmor, M. F.: Contributions of the sodium pump and ionic gradients to the membrane potential of a molluscan neurone. J. Physiol. (Lond.)210, 897–917 (1970).

    Google Scholar 

  • Harvey, A. A., MacIntosh, F. C.: Calcium and synaptic transmission in a sympathetic ganglion. J. Physiol. (Lond.)97, 408–416 (1940).

    Google Scholar 

  • Hayes, F. R., Pelluet, D.: Inorganic constituents of molluscs. J. Mar. Biol. Ass. U. K.26, 580–589 (1947).

    Google Scholar 

  • Hodgkin, A. L., Huxley, A. F.: The dual effect of membrane potential on sodium conductance in the giant axon ofLoligo. J. Physiol. (Lond.)116, 497–506 (1952).

    Google Scholar 

  • Hodgkin, A. L., Keynes, R. D.: The potassium permeability of a giant nerve fibre. J. Physiol. (Lond.)128, 61–88 (1955).

    Google Scholar 

  • Hoyle, G.: The effects of some common cations on neuromuscular transmission in insects. J. Physiol. (Lond.)127, 90–103 (1955).

    Google Scholar 

  • Hughes, H. P. I.: A light and electron microscope study of some opistho-branch eyes. Z. Zellforsch.106, 79–98 (1970).

    Google Scholar 

  • Jacklet, J. W.: Circadian rhythm of optic nerve impulses recorded in darkness from is-lated eye ofAplysia. Science164, 562–563 (1969a).

    Google Scholar 

  • Jacklet, J. W.: Electrophysiological organization of the eye ofAplysia. J. gen. Physiol.53, 21–42 (1969b).

    Google Scholar 

  • Jacklet, J. W.: Circadian rhythm in the activity of a population of coupled neurons. Fed. Proc.30, 551 (1971).

    Google Scholar 

  • Jacklet, J. W., Alvarez, R., Bernstein, B.: Ultrastructure of the eye ofAplysia. J. Ultrastruct. Res.38, 246–261 (1972).

    Google Scholar 

  • Jacklet, J. W., Geronimo, J.: Circadian rhythm population of interacting neurons. Science174, 299–302 (1971).

    Google Scholar 

  • Katz, B., Miledi, R.: A study of synaptic transmission in the absence of nerve impulses. J. Physiol. (Lond.)192, 407–463 (1967).

    Google Scholar 

  • Kerkut, G. A., Meech, R. W.: The effect of ions on the membrane potential of snail neurones. Comp. Biochem. Physiol.20, 411–429 (1967).

    Google Scholar 

  • Kernan, R. P.: Cell K, Washington, D. C.: Butterworth, Inc. 1965.

    Google Scholar 

  • Miledi, R., Slater, C. R.: The action of calcium on neuronal synapses in the squid. J. Physiol. (Lond.)184, 473–498 (1966).

    Google Scholar 

  • Pavlidis, T.: Populations of interacting oscillators and circadian rhythms. J. theoret. Biol.22, 418–436 (1969).

    Google Scholar 

  • Pittendrigh, C. S., Minis, D. H.: The entrainment of circadian oscillations by light and their role as photoperiodic clocks. Amer. Nat.93, 261–294 (1964).

    Google Scholar 

  • Rall, T. W., Sattin, A.: Factors influencing the accumulation of cyclic AMP in brain tissue. Adv. Biochem. Psychopharm.3, 113–133 (1970).

    Google Scholar 

  • Rubin, R. P.: The role of calcium in the release of neurotransmitter substances and hormones. Pharmacol. Rev.22, 389–428 (1970).

    Google Scholar 

  • Ruch, T. C., Patton, H. D., Woodbury, J. W., Towe, A. L.: Neurophysiology (2 ed.). Philadelphia: W. B. Saunders Co. 1965.

    Google Scholar 

  • Sato, M., Austin, G., Yai, H., Maruhashi, J.: The ionic permeability changes during acetylcholine-induced responses ofAplysia ganglion cells. J. gen. Physiol.51, 321–345 (1968).

    Google Scholar 

  • Shimizu, H., Creveling, C. R., Daly, J. W.: Effect of membrane depolarization and biogenic amines on the formation of cyclic AMP in incubatied brain slices. Adv. Biochem. Psychopharm.3, 135–154 (1970).

    Google Scholar 

  • Sjodin, R. A., Beauge, L. A.: Coupling and selectivity of sodium and potassium transport in squid giant axons. J. gen. Physiol.51 (Part 2), 152–161s (1968).

    Google Scholar 

  • Strumwasser, F.: The demonstration and manipulation of a circadian rhythm in a single neuron, p. 442–462. In: Circadian clocks (J. Aschoff, ed.). Amsterdam: North-Holland Publ. Co. 1965.

    Google Scholar 

  • Winfree, A. T.: Integrated view of resetting a circadian clock. J. theoret. Biol.28, 327–374 (1970).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Biology, California Institute of Technology, 91109, Pasadena, California

    A. Eskin

  2. Biology Department, Rice University, 77001, Houston, Texas, USA

    A. Eskin

Authors
  1. A. Eskin
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Dedicated to Professor Jürgen Aschoff on the occasion of his 60th birthday for the important role he has played in generating the current interest in circadian rhythm research.

I am very grateful to Dr. Felix Strumwasser for providing excellent facilities for this research and for helpful suggestions during the course of this work and the writing of this manuscript. I thank Mr. Dave Peisner for his assistance in performing preliminary experiments on the effects of hi-K pulses on the eye ofAplysia. I thank Mr. James Gilliam for his skillful technical assistance and Drs. S. Arch, D. L. Wilson, and Mr. J. Ram for helpful discussions. This work was supported in part by USPHS Postdoctoral Fellowships (1-F2-GM-33,240-01 and 2-F02-GM-32,240,02) and grants from NIH (NS 07071), NASA (NGR 05-002-031), and the Alfred P. Sloan Foundation to Dr. F. Strumwasser.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Eskin, A. Phase shifting a circadian rhythm in the eye ofAplysia by high potassium pulses. J. Comp. Physiol. 80, 353–376 (1972). https://doi.org/10.1007/BF00696434

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00696434

Keywords

Search

Navigation